Prasinophytes are widespread marine algae for which responses to nutrient limitation and viral infection are not well understood. We studied the picoprasinophyte, Micromonas pusilla, grown under phosphate‐replete (0.65 ± 0.07 d−1) and 10‐fold lower (low)‐phosphate (0.11 ± 0.04 d−1) conditions, and infected by the phycodnavirus MpV‐SP1. Expression of 17% of Micromonas genes in uninfected cells differed by >1.5‐fold (q < 0.01) between nutrient conditions, with genes for P‐metabolism and the uniquely‐enriched Sel1‐like repeat (SLR) family having higher relative transcript abundances, while phospholipid‐synthesis genes were lower in low‐P than P‐replete. Approximately 70% (P‐replete) and 30% (low‐P) of cells were lysed 24 h post‐infection, and expression of ≤5.8% of host genes changed relative to uninfected treatments. Host genes for CAZymes and glycolysis were activated by infection, supporting importance in viral production, which was significantly lower in slower growing (low‐P) hosts. All MpV‐SP1 genes were expressed, and our analyses suggest responses to differing host‐phosphate backgrounds involve few viral genes, while the temporal program of infection involves many more, and is largely independent of host‐phosphate background. Our study (i) identifies genes previously unassociated with nutrient acclimation or viral infection, (ii) provides insights into the temporal program of prasinovirus gene expression by hosts and (iii) establishes cell biological aspects of an ecologically important host‐prasinovirus system that differ from other marine algal‐virus systems.